Withholding a Reward-driven Action: Studies of the Rise and Fall of Motor Activation and the Effect of Cognitive Depletion.

Abstract

Controlling an inappropriate response tendency in the face of a reward-predicting stimulus likely depends on the strength of the reward-driven activation, the strength of a putative top-down control process, and their relative timing. We developed a rewarded go/no-go paradigm to investigate such dynamics. Participants made rapid responses (on go trials) to high versus low reward-predicting stimuli and sometimes had to withhold responding (on no-go trials) in the face of the same stimuli. Behaviorally, for high versus low reward stimuli, responses were faster on go trials, and there were more errors of commission on no-go trials. We used single-pulse TMS to map out the corticospinal excitability dynamics, especially on no-go trials where control is needed. For successful no-go trials, there was an early rise in motor activation that was then sharply reduced beneath baseline. This activation-reduction pattern was more pronounced for high- versus low-reward trials and in individuals with greater motivational drive for reward. A follow-on experiment showed that, when participants were fatigued by an effortful task, they made more errors on no-go trials for high versus low reward stimuli. Together, these studies show that, when a response is inappropriate, reward-predicting stimuli induce early motor activation, followed by a top-down effortful control process (which we interpret as response suppression) that depends on the strength of the preceding activation. Our findings provide novel information about the activation-suppression dynamics during control over reward-driven actions, and they illustrate how fatigue or depletion leads to control failures in the face of reward.

On Go trials (left panel), continuous presses were made in effort to receive points (later converted to money). If enough presses were made on a given trial, the earned points were displayed to the participant; otherwise, no points were displayed and the next trial began. The amount of potential points to be earned on a given trial was indicated by the background color. One color (shown as yellow here) was associated with substantially higher point rewards than the other color (shown as blue here). On NoGo trials (right panel), responding was to be withheld; else, a red error message appeared. Go and NoGo trials were equiprobable. (B) On Go trials, the first press reaction time was significantly faster for high compared to low reward trials. (C) On Go trials, more presses were made for high compared to low reward trials. (D) On NoGo trials, the error rate was significantly greater for high compared to low reward trials. This indicates that the high reward background stimulus provoked responding on both Go and NoGo trials. Error bars represent SEM across participants. ***p < 0.001.

(A) High reward Go trials showed a linear increase in motor excitability across the four time points. Low reward Go trials showed an initial decrease in motor excitability (from 100–200 ms), followed by an increase from 200–250 ms. (B) On NoGo trials, high and low reward showed an initial increase in motor excitability from 100–150 ms (activation phase), followed by a decrease from 150–250 ms (reduction phase). (C) On NoGo trials, the percent-change for the reduction phase was twice as strong (measured via effect size) for high versus low reward trials and only high reward trials showed a significant difference between percent-change in the activation and reduction phases. (D) On NoGo trials, greater reward-based (i.e. high minus low reward) activation was related to greater reward-based suppression. Error bars represent SEM across participants. ^p < 0.06, *p < 0.05, ***p < 0.001. All p-values are adjusted according to a Holm-Bonferroni correction.

(A) Go trial dynamics. High reward Go trials showed an increase in motor excitability across all four time points, while low reward Go trials showed a decrease from 100–200 ms, followed by an increase from 200–250 ms. High and low reward Go trials in the slow RT group largely resembled that of the fast RT group. (B) High reward NoGo trials in the fast RT group showed an initial steep increase (from 100–150 ms), followed by a sharp decrease (from 150–250 ms). This pattern was markedly different than low reward NoGo trials, which did not show the initial increase and also a less steep decrease. In contrast to the fast RT group, the slow RT group showed no differences in motor excitability between high and low reward NoGo trials during the activation and reduction phases. Follow-up analyses showed that group differences in the reward motor dynamics were only in the 150 ms time point. Error bars represent SEM across participants. ## = p < 0.05 for Reward × Pulse Time × Group interaction, # = p < 0.05 for Reward × Group interaction.

Percent-change across time points for fast and slow RT groups on NoGo trials Experiment 1

(A) During the activation phase, the fast and slow RT groups showed different reward motor dynamics, resulting in a significant Group × Reward interaction. Specifically, the fast RT group showed greater sensitivity to the high versus low reward stimulus. (B) During the reduction phase, there was also a significant Group × Reward interaction, where the fast RT group again showed greater sensitivity to the high versus low reward stimulus. (C) The fast RT group showed a significant correlation between the degree of reward-based (i.e. high minus low reward) activation and reward-based reduction. (D) The correlation for the slow RT group did not reach significance; further, a Fisher’s r-to-z transform test revealed that the correlation for the fast RT group was significantly greater than the slow RT group. Error bars represent SEM across participants. #p < 0.05 for Reward × Group interaction.

(A) There were 3 parts in the task. In part 1, participants completed the rewarded Go/NoGo task (as in Experiment 1). This provided a baseline measurement for each participant’s NoGo error rate on high and low reward trials. In part 2, participants either completed a cognitively demanding three-back working memory task (High load) or a less demanding zero-back task (Low load). For the zero-back task, they were required to press a button (indicated by a red outline) whenever they saw the letter “P”. For the three-back task, they were required to press a button whenever the current letter matched the letter presented three letters before. In part 3, participants completed another rewarded Go/NoGo task to examine the change in error rates on high and low reward NoGo trials following the WM manipulation. (B) A proportion correct measurement shows that the high load (three-back) task was significantly more difficult than the low load (zero-back) task. (C) Only high reward trials in the High load group showed a significant increase in the error rate following the WM manipulation. This increase was significantly greater than the low reward trials in the High load group. The Low load group showed no difference between high and low reward NoGo trials and no pre-post changes in error rates. Error bars represent SEM across participants. *p < 0.05, ***p < 0.001.